The phylogenetic distribution of resupinate forms across the major ...

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12 Manfred Binder et al. 100 Cyclomyces fuscus CBS 100.106 Cyclomyces tabacinus CBS 311.39 Stipitochaete damaecornis DSH 98-006 Hymenochaet e adusta TAA 95-37 Hymenochaet e bertero i CBS 733.86 Hymenochaet e pseudoadusta TAA 95-38 Hymenochaet e boidini i CBS 762.91 Hymenochaet e separabilis CBS 738.86 Hymenochaet e rhabarbarina GEL4809 Hymenochaet e ochromarginat a CBS 928.96 Hymenochaet e rubiginos a TW 22.9.97 Hymenochaet e cinnamome a LK 27.9.97 Hymenochaet e nanospor a CBS 924.96 Hymenochaet e fuliginos a CBS 933.96 Hymenochaet e carpatic a TW 27.9.97 Hymenochaet e separat a TAA 95-24 Hymenochaet e cruenta HB 149/80 Hymenochaet e denticulat a CBS 780.91 Hymenochaet e pinnatifida CBS 770.91 Hydnochaet e duporti i CBS 941.96 Hydnochaete japonica CBS 499.76 Hymenochaet e acanthophysat a CBS 925.96 Hymenochaet e cervinoide a CBS 736.86 Phellinus igniarius FPL-5599 Phellinus lundellii TN 5760 Phylloporia ribis FPL-10677 Phellinus laevigatus TN 3260 Phellinus conchatus 89-1014 Inonotus hispidus FPL-3597 Mensulari a hastifera 84-1023a Hymenochaet e corrugata FP-104124-Sp. Pseudochaet e tabacina LK 12.10.97 Hydnochaet e olivacea CLA 02-003 Fomitiporia punctata 85-74 Onnia triquetra TW 411 Fuscoporia contigua TW 699 Phellinus gilvus FPL-5528 Fuscoporia torulosa Pt 4 Fuscoporia ferruginosa 82-930 Fuscoporia ferrea 87-8 Coltricia montagnei 96-96 Coltricia perennis DSH 93-198 Phellinidiu m ferrugineofuscum TN 612 1 Asterodon ferruginosus Dai 3186 Phellopilus nigrolimitatus 85-823 Tubulicrini s gracillimus HHB-13180-Sp. Tubulicrini s subulatus GEL5286 Basidioradulum radula FO-23507a Fibricium rude GEL212 1 Trichaptum abietinum FPL-8973 Hyphodontia alutacea GEL2937 Hyphodontia niemelaei GEL5068 Schizopora radula GEL3798 Hyphodontia serpentiformis GEL3307 Schizopor a paradoxa GEL2511 Hyphodontia nudiset a GEL5302 Hyphodontia aff. breviset a GEL4214 Hyphodontia nespor i GEL4190 Hyphodontia crustos a GEL5360 Hyphodontia sambuc i GEL2414 Hyphodontia aspera GEL2135 Repetobasidium mirificiu m FP-133558-Sp. Sphaerobasidium minutum GEL5373 “H yphodontia alutaria”? GEL2071 Resinicium bicolor FP-135104-Sp . Hyphodontia palmae GEL3456 Hyphodontia cineracea GEL4875 Hyphodontia pallidul a GEL4533 Schizopor a flavipor a GEL3545 Hyphodontia alutari a GEL4553 Oxyporus populinus FO35584 Tubulicrini s sp. GEL5046 Subuliciu m sp. GEL4808 Resinicium meridionale FP-150236 Trechispor a araneosa KHL 8570 Trechispor a sp. KHL 10715 Trechispor a confinis KHL 11064 Trechispor a subsphaerospor a KHL 8511 Trechispor a incisa EH 24/98 Trechispor a kavinioide s KGN 981002 Trechispor a hymenocystis KHL 8795 Trechispor a regulari s KHL 10881 Trechispor a farinacea KHL 8451 Trechispor a farinacea KHL 8454 Trechispor a farinacea KHL 8793 Hyphodontia gossypin a GEL5042 Subulicystidiu m longisporum GEL3550 Porpomyces mucidus KHL 8471 Porpomyces mucidus KHL 8620 Porpomyces mucidus KHL 11062 Tubuliciu m vermiculare GEL5015 Sistotremastru m niveocremeu m FO29191 Sistotremastru m niveocremeum EL 96-97 Sistotremastru m sp. FO36293b Anthurus archeri GEL5392 Pseudocolus fusiformis DSH 96-033 Gastrosporium simplex WÜ2768 Hysterangium stoloniferum WÜ3706 Geastrum saccatum DSH 96-048 Geastrum sessile GEL5319 Sphaerobolus stellatus DSH 96-015 Ramaria stricta TENN HDT-5474 Gautieria otthii REG636 Gomphus floccosus DSH 94-002 Ramaria formosa M-95 Ramaria obtusissima GEL4416 Clavariadelphus ligulus KHL 8560 Clavariadelphus pistillaris n/a Lentaria micheneri RV98/147 Ramaricium alboflavescen s DAOM 17712 Kavini a himantia FP-101479 Hydnum repandum DSH 97-320 Hydnum rufescens MB18-6024/1 Hydnum albidum MB11-6024/2 Sistotrem a brinkmanni i GEL3134 “S istotremastru m niveocremeum” ? FO36914 Multiclavula mucida DSH 96-056 Clavulina cinerea 33 Sistotrema eximum RGT42 0 Sistotrem a sernanderi CBS 926.70 Botryobasidium subcoronatum GEL4673 Botryobasidium subcoronatum GEL5397 Botryobasidium subcoronatu m FCUG 1286 Botryobasidium agg. vagum GEL4181 Botryobasidium vagum GEL212 2 Botryobasidium isabellinum GEL2108 Botryobasidium isabellinum GEL2109 Botryobasidium sp. GEL4968 Botryobasidium sp. GEL5132 Botryobasidium agg. candican s GEL2090 Botryobasidium candican s GEL3083 Ceratobasidium sp. GEL 5602 Uthatobasidium sp. FO30284 Uthatobasidium fusisporum HHB-102155-Sp. Thanatephorus praticola IMI-34886 Tulasnella pruinos a DAOM 17641 Tulasnella viole a DAOM 222001 Tulasnella sp. GEL4461 Tulasnella sp. GEL4745 Piriformospora indica DSM 11827 Serendipita vermifera CBS 572.83 Pseudohydnum gelatinosum DSH 97-041 Auricularia auricula-judae GJW-855-10 Exidiopsis calcea HHB-15059-Sp. Exidia thuretiana GEL5242 Heterochaet e sp. GEL4813 Basidiodendron sp. GEL4674 Bourdotia sp. GEL4777 Basidiodendron caesiocinereu m GEL5361 Calocera cornea FP-102602-Sp. Cerinomyces grandinioide s GEL4761 Dacryopinax spathularia GEL5052 Dacrymyces sp. GEL5083 Dacrymyces stillatus GEL5264 Dacrymyces chrysospermus FPL11353 Ditiola radicata GEL4014 Dacryomitra pusilla FO38346 Femsjonia sp. FO28211 Guepinia spathularia FO45821 Figure 4 For Legend see facing page. A 69 69 Auriculariales s. str. Dacrymycetales Hymenochaetaceae trechisporoid clade gomphoid-phalloid clade bootstrap 65-79% 80-89% 90-100% 50 changes hymenochaetoid clade Resinicium meridionale Cantharellus tubaeformis DSH 93-209 Craterellus cornucopioides DSH 96-003 Cantharellus cibarius n/a cantharelloid clade
To compare results of the present study with those of Weiß & Oberwinkler (2001), the sequences of Sebacinaceae, Ceratobasidium pseudocornigerum, Ceratosebacina calospora and other taxa were downloaded, combined with a subset of sequences from the present study, and subjected to bootstrapped parsimony analyses (Hibbett, unpublished). The sequences of Sebacinaceae from the study of Weiß & Oberwinkler (2001) and Serendipita vermifera from the present study were moderately strongly supported as a clade (bootstrap = 89%), confirming that S. vermifera is an appropriate ‘placeholder’ for the Sebacinaceae, but Ceratobasidium pseudocornigerum and Ceratosebacina calospora could not be placed in any clade with confidence (bootstrap < 50 %, Hibbett, unpublished). These results suggest that the Ceratobasidiales as presently delimited could be polyphyletic. In addition, analyses of mt-lsu rDNA by Bruns et al. (1998) suggested that Waitea circinata, which is placed in the Ceratobasidiales (Tu et al., 1977; Roberts, 1999), is closely related to the resupinate homobasidiomycete Piloderma croceum,which is probably a member of the athelioid clade (see below). Conflicting results were obtained by DePriest and colleagues (unpublished), who performed analyses of ITS and partial nuclsu rDNA sequences that suggested that Waitea circinata is in the corticioid clade (see below). The placement of Waitea will remain unresolved until additional loci and isolates are examined. Nevertheless, neither of the analyses cited above suggest that it is closely related to the cantharelloid clade. The isolates of Ceratobasidium, Thanatephorus and Uthatobasidium included in the present study are strongly supported as monophyletic and are placed in the cantharelloid clade in the PR analyses. Bootstrap support for the cantharelloid clade is weak in the full dataset analyses, but in the core dataset analysis, Ceratobasidium sp. is nested in the cantharelloid clade, with moderately strong bootstrap support (85%, Figs 1, 4). Taking the results of previous studies into account, the Ceratobasidiales as a whole may be polyphyletic, but Ceratobasidium, Thanatephorus and Uthatobasidium appear to form a monophyletic group within the cantharelloid clade. Serendipita vermifera is strongly supported as the sister group of the root symbiont Piriformospora indica (Verma et al., 1998) and the Serendipita–Piriformospora clade is placed as the sister group of the Tulasnellales, in the cantharelloid clade (Fig. 4). Monophyly of the Serendipita–Piriformospora–Tulasnellales clade is weakly supported (Fig. 4). Nevertheless, these results are consistent with the results of mt-lsu rDNA analysis by Bruns et al. (1998), which resolved a clade that includes Tulasnella irregularis and “Sebacina sp.” and placed it as the sister group of Cantharellus with strong (98%) Phylogenetic distribution of resupinate forms of mushroom-forming fungi 13 bootstrap support (also see Kristiansen et al., 2001). Weiß & Oberwinkler (2001) did not include Tulasnellales in their analyses of nuc-lsu rDNA sequences, but they cited unpublished analyses of nuc-ssu rDNA sequences, which apparently placed the Tulasnellales near the Auriculariales. In contrast, E. Langer (1998) found strong support (bootstrap = 95%) for a clade including Tulasnella eichleriana and two species of Botryobasidium, which is a member of the cantharelloid clade (see below), based on mt-ssu rDNA sequences. In addition, Kottke et al. (2003) and Bidartondo et al. (2003) found moderately strong (bootstrap = 88–89%) support for a clade including three species of Tulasnella, several liverwort symbionts, and Multiclavula mucida, which is also a member of the cantharelloid clade, based on nuc-lsu rDNA sequences. Comparable results were obtained by Hibbett & Binder (2002) and Hibbett & Donoghue (2001). Tulasnellales have highly divergent nuclear rDNA sequences (Weiß & Oberwinkler, 2001; Hibbett, unpublished), so it is possible that the results described by Weiß and Oberwinkler are due to ‘long branch attraction’. Basal Homobasidiomycetes The cantharelloid clade, gomphoid-phalloid clade and hymenochaetoid clade appear to be among the earliest-diverging groups in the Homobasidiomycetes (Figs 1, 3, 4). In addition, the trechisporoid clade is placed as the sister group of the hymenochaetoid clade in one of the topologies obtained with six-parameter weighted PR analysis (Figs 3, 4). Bootstrap support for the placements of these clades are weak (Figs 1, 4), but ultrastructural characters of septal pores are consistent with the view that they occupy basal positions. Imperforate parenthesomes have been found in the cantharelloid clade (Botryobasidium, Cantharellus, Piriformospora, Sebacina, Tulasnella), gomphoid-phalloid clade (Geastrum, Ramaria), hymenochaetoid clade (Basidioradulum, Coltricia, Hymenochaete, Hyphodontia, Schizopora, Trichaptum, etc.), and trechisporoid clade (Hyphodontia gossypina, Subulicystidium longisporum), as well as the Auriculariales and Dacrymycetales (Traquair & McKeen, 1978; Moore, 1980; 1985; G. Langer, 1994; Verma et al., 1998; Müller et al., 2000; Hibbett & Thorn, 2001; Wells & Bandoni, 2001; E. Langer, 2002; K.-H. Larsson et al., 2004). Most other Homobasidiomycetes have perforate parenthesomes (examples are known in the euagarics, polyporoid, bolete, thelephoroid and russuloid clades), which probably represent a derived condition (E. Langer, 1998; Hibbett & Thorn, 2001; E. Langer, 2002). However, imperforate parenthesomes have been reported in the polyporoid clade (Phanerochaete sordida) and perforate parenthesomes have been reported in the gomphoid-phalloid clade (Clathrus), cantharelloid Figure 4 Phylogenetic distribution of resupinate forms among the Homobasidiomycetes, based on six-parameter weighted PR analyses of the full 656-OTU dataset. This phylogram represents topology G (Fig. 3); see figure for branch length scale. Ranges of bootstrap values obtained using equally weighted parsimony greater than 65% are indicated with shaded dots on branches (white = 65–79%; grey = 80–89%; black = 90–100%). Exact bootstrap values for major clades are also written along branches, where they are above 50%. Species names are followed by strain numbers that were used to generate 25S sequences. Species names in quotation marks followed by question marks indicate mislabelled isolates. Names of resupinate taxa are written in bold type. Major clades of Homobasidiomycetes are indicated with brackets. This is part of the phylogenetic tree, including Dacrymycetales, Auriculariales and basal clades of Homobasidiomycetes.
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